Case study 2: Improving water and nutrient acquisition in
dryland cereals in West Africa
Sorghum (Sorghum bicolor [L.] Moench) and pearl millet
(Pennisetum glaucum [L.] R. Br.) are the fifth and sixth most
important cereal crop in the World
(FAOSTAT
2007; FAO 2014).
They are well adapted to arid and semi-arid environments found in
sub-Saharan Africa and India. In these regions, they are usually grown
one cycle a year during the rainy season by smallholder farmers and
represent a major source of micronutrient protein for humans and fodder
for livestock. They are usually sown at low density (around 10,000
plants per
hectare,FAO
2012) before or right after the first rain of the season and grown with
no or low inputs simply because water and fertilizers are inaccessible
and/or unaffordable
(Matlon 1990; vom
Brocke et al. 2010). Although sorghum and pearl millet prevail in
these environments where other mainstream crops tend to fail, their
cultivation is increasingly threatened by high temperature and
intermittent drought caused by climate change and soil degradation
caused by loss of nutrients and soil organic carbon, a phenomenon
accentuated by desertification and erosion
(Jones et
al. 2013; Sultan, Defrance & Iizumi 2019). Therefore, improving the
resilience of sorghum and pearl millet is particularly important for
food security in arid and semi-arid regions of Africa and for adaptation
of African agriculture to future climates.
Sorghum and pearl millet root systems are characterized by a single
primary root and multiple post-embryonic nodal roots that originate from
the mesocotyl
(Tsuji et
al. 2005; Chopart, Sine, Dao & Muller 2008; Singh et al. 2010;
Faye et al. 2019). Primary, seminal and nodal roots all have
lateral roots. In pearl millet, three different types of lateral roots
have been identified that differ by length, diameter and internal
structures
(Passot et
al. 2016), as well as by their growth dynamics
(Passot et
al. 2018). In sorghum, large variability in crown root angle and root
area was observed in diversity panels, backcross nested association
mapping (BCNAM) populations and recombinant inbred lines
(Mace et
al. 2012; Joshi et al. 2017). Similarly, diversity in primary
root growth and root branching
(Passot et
al. 2016), and root length density
(Faye et
al. 2019) was observed in pearl millet. Despite this observed root
phenotypic diversity and the fact that several authors have proposed
root phenes as breeding targets for improvement of sorghum and pearl
millet (Gemenetet al. 2016; Joshi et al. 2016), selection strategies
involving root phenes have not been deployed to improve their
cultivation so far.
For sorghum and pearl millet grown in sub-Saharan Africa where soils are
generally deep and sandy with low water retention, deep rooting might be
particularly interesting for tolerance to drought stress
(Joshi et
al. 2016). In maize, reducing crown root number or lateral root density
was associated with deeper root growth, greater water capture at depth
and improved plant water status and yield under drought
(Zhan, Schneider
& Lynch 2015; Gao & Lynch 2016). This response is linked to a carbon
allocation mechanism in which plants that develop fewer roots are able
to invest more carbon in individual roots that can grow deeper
(Lynch 2013,
2018; Van Oosterom et al. 2016). Another means for a plant to
grow deeper roots is to develop nodal roots with steeper growth angle
(Lynch 2013). In
sorghum, QTLs for steep nodal root angle co-located with QTL previously
identified for stay-green and were associated with grain yield
(Mace et
al. 2012; Borrell et al. 2014).
Reduced root cortical cell file number (CCFN) and cortical cell size
(CCS) were also hypothesized to reduce the metabolic cost of soil
exploration
(Lynch 2018).
Maize lines with lower CCFN and greater CCS showed reduced root
respiration, increased root growth at depth, better shoot growth and
water status, and significant increase in yield under drought as
compared to lines with more CCFN and less CCS
(Burton, Brown &
Lynch 2013; Jaramillo, Nord, Chimungu, Brown & Lynch 2013; Chimungu,
Brown & Lynch 2014a,b). Similarly, maize lines with more root cortical
aerenchyma (RCA) showed decreased root respiration, increased deep
rooting, shoot growth and yield
(Zhu, Brown &
Lynch 2010; Chimungu et al. 2015). Moreover, simulations using
the functional-structural plant model OpenSimRoot showed that more RCA,
less CCFN and lower CCS had beneficial effects on plant biomass after 42
days of growth under nitrogen (N), P and potassium (K) stresses
(Postma et
al. 2017; Lynch 2019). RCA formation was observed both in sorghum and
pearl millet indicating that this phene could be explored for diversity,
genetic control and used for improving drought tolerance
(Promkhambut,
Polthanee, Akkasaeng & Younger 2011; Jaffuel et al. 2016; Passotet al. 2016). No information exists however on CCFN and CCS
diversity nor their impacts in sorghum and pearl millet drought
response.
If drought tolerance is often dependent on the ability for the plant to
capture water, it is equally dependent on the way this water is used to
produce biomass, i.e. its transpiration efficiency. Strategies to
improve transpiration efficiency have sometimes relied on reduced xylem
conductance capacity. In wheat for instance, reduced xylem diameter and
the associated reduced root hydraulic conductance resulted in more
conservative plants that yielded 11% more grains under drought
conditions
(Richards &
Passioura 1989). In fact, annual crop plants adapted to drought stress
environments tend to favour smaller xylem diameter as a water
conservation strategy
(Henry, Cal,
Batoto, Torres & Serraj 2012; Kadam, Yin, Bindraban, Struik & Jagadish
2015; Grondin, Mauleon, Vadez & Henry 2016). Sorghum lines with higher
number of xylem vessels showed higher transpiration rate which suggest
that reducing xylem vessel number in this crop could lead to water
saving strategies
(Salih et
al. 1999). The ability for a plant to restrict transpiration when the
vapor pressure deficit (VPD) is above a certain threshold (transpiration
restriction) represents other means for improving transpiration
efficiency
(Sinclairet al. 2017). In sorghum, simulations suggested that restricting
maximum transpiration would increase transpiration efficiency and
sustain physiological activities and yield
(Sinclair 2005).
Large variability for this transpiration restriction phenotype was
observed in sorghum and in pearl millet
(Kholová et
al. 2010; Reddy et al. 2017; Tharanya et al. 2018;
Karthika et al. 2019). In pearl millet, transpiration restriction
was recently linked with root and shoot aquaporins expression although
their precise function in this mechanism remains largely unknown
(Reddy et
al. 2017; for review see Shekoofa & Sinclair 2018; Tharanya et
al. 2018). Improving transpiration efficiency (biomass/water
transpired) over the entire crop cycle, possibly by restricting maximum
transpiration at high VPD through reduction in root xylem size and
possibly modulation in aquaporin functions could well conserve soil
water for the critical reproduction and grain filling stage
(Kholová et
al. 2010; Vadez, Kholová, Yadav & Hash 2013; Vadez 2014).
Root hairs are well-known to improve P acquisition from the soil by
increasing the absorption area of the root system
(Lynch 2019). In
sorghum and pearl millet, characterization of root hair density and
length, genotypic variation, as well as their role in P uptake, remains
limited. Recent study of the genetic architecture of phosphorus
efficiency in sorghum showed colocalization between QTL for P
acquisition efficiency, grain yield, surface area and root diameter
(Bernadino et al., 2019). Interestingly, one QTL located on chromosome 3
was in close physical proximity with the sorghum homolog of rice
serine/threonine kinase OsPSTOL1 , which was previously found to
enhance early root growth and grain yield in rice under low-P
(Gamuyao et
al. 2012; Bernardino et al. 2019). Increasing exploration of
shallow soil by increasing root length density or by increasing root
hair length and density might be beneficial for P capture. In addition,
benefits from more root hairs of sorghum could come from their
contribution to the synthesis and exudation of sorgoleone that have
demonstrated roles in growth inhibition of weeds
(Netzly & Butler
1986; Pan et al. 2018).
There are clear trade-offs between root phenes beneficial for drought
and low-P tolerance. In environments where P scarcity is always a
constraint but drought is often intermittent, increased top-soil root
hair length and density combined with drought-inducible plasticity in
deeper root growth possibly through reduced top-soil root carbon cost
(more RCA for instance) could co-optimize drought and low-P tolerance
(Fig. 2B). Drought-related root plastic response has been described inSetaria italica (a close relative of sorghum and pearl millet),
where an interruption in crown root growth under drought was observed
(Sebastianet al. 2016). This plastic response appeared to be conserved in
sorghum and pearl millet where nodal root length was significantly
reduced when grown in split-pot system where the seminal root grew in
moist soil while the crown roots grew in dry soil
(Rostamza,
Richards & Watt 2013). These observations suggest that root plasticity
in response to drought exists, and could be exploited to improve
drought-tolerance. Intercropping systems where root systems of
neighbouring plants (sorghum/pearl millet and cowpea/groundnut for
instance) could have complementary interactions in terms of water and
nutrient availability without competing with each other may also help
reducing these trade-offs
(Brooker et
al. 2015).
Beyond root architectural and anatomical phenes, targeting the
rhizosphere could be another future avenue to improve dryland cereals
performance (de
la Fuente Cantó et al. 2020). The rhizosphere is the volume of
soil around the root under the influence of the root system, i.e. whose
physico-chemical and biological properties are modified by the root,
which, in turn, impacts plant nutrition, development and physiology
(York, Carminati,
Mooney, Ritz & Bennett 2016; de la Fuente Cantó et al. 2020).
One potential rhizosphere target phene in sorghum and pearl millet would
be rhizosheath formation, i.e. the aggregation of soil particles around
the roots (Ndour,
Heulin, Achouak, Laplaze & Cournac 2020). This fraction of the soil
firmly attached to the roots corresponds to the most biologically active
fraction of the rhizosphere. First described in desert grasses,
rhizosheath formation has since been reported in many cereal crops
including sorghum and pearl millet
(Duell & Peacock
1985; Brown, George, Neugebauer & White 2017; Ndour et al.2017b). A positive impact on water and mineral nutrition was reported
for several plants in laboratory conditions and could be in part
explained by improved contact between the soil and the root surface
(Ndour et
al. 2020). Phenotyping for rhizosheath size is high throughput and this
phene is largely under plant genetic control and large variability
exists in the germplasm in pearl millet thus making it a potential
target for breeding
(Ndour et
al. 2021). However, further work is needed to demonstrate the impact of
a larger rhizosheath on dryland cereals in field conditions.